Bottom Line:
To understand how the underlying neural network controls this behavior, it is not sufficient to unravel its architecture, but also crucial to decipher its logic.By systematic analysis of how variations in sensory inputs alter the courtship behavior of a naïve male in the single-choice courtship paradigm, we derive a model describing the logic of the network that integrates the various sensory stimuli and elicits this complex innate behavior.This approach and the model derived from it distinguish (i) between initiation and maintenance of courtship, (ii) between courtship in daylight and in the dark, where the male uses a scanning strategy to retrieve the decamping female, and (iii) between courtship towards receptive virgin females and mature males.

Affiliation: Institute for Molecular Biology, University of Zürich, Zürich, Switzerland.

ABSTRACTThe courtship behavior of Drosophila melanogaster serves as an excellent model system to study how complex innate behaviors are controlled by the nervous system. To understand how the underlying neural network controls this behavior, it is not sufficient to unravel its architecture, but also crucial to decipher its logic. By systematic analysis of how variations in sensory inputs alter the courtship behavior of a naïve male in the single-choice courtship paradigm, we derive a model describing the logic of the network that integrates the various sensory stimuli and elicits this complex innate behavior. This approach and the model derived from it distinguish (i) between initiation and maintenance of courtship, (ii) between courtship in daylight and in the dark, where the male uses a scanning strategy to retrieve the decamping female, and (iii) between courtship towards receptive virgin females and mature males. The last distinction demonstrates that sexual orientation of the courting male, in the absence of discriminatory visual cues, depends on the integration of gustatory and behavioral feedback inputs, but not on olfactory signals from the courted animal. The model will complement studies on the connectivity and intrinsic properties of the neurons forming the circuitry that regulates male courtship behavior.

pone-0004457-g004: Gustatory, but not olfactory, signals of the courted fly contribute to the heterosexual orientation of the courting male.(A) The fraction of males initiating courtship, (B) the average latency (in seconds) till courtship initiation, and (C) the courtship vigor index were measured in single-choice courtship assays, performed under dim red light with courting males of indicated genotypes and decapitated receptive Ore-R virgins (V, filled columns) or decapitated mature Ore-R males (♂, hatched columns).

Mentions:
To assess the importance of the different senses for the sexual orientation of males, we first observed males in single-choice courtship assays in the dark with object animals that had been decapitated to prevent their feedback behavior. All Ore-R and Poxn-SuperA control males initiated courtship towards decapitated females (Figure 4A) with a short latency (Figure 4B) and courted them vigorously until the end of observation (Figure 4C). Copulation with decapitated females was never observed even though males bent their abdomen and attempted to copulate, which suggests that positive feedback from the female is crucial for copulation (M13). When confronted with decapitated males, the fraction of Ore-R and Poxn-SuperA males initiating courtship was somewhat reduced (Figure 4A; p = 0.008 and p = 0.1, respectively, for comparison of courtship towards decapitated females and males), and the courtship latency significantly increased (Figure 4B; p = 0.006 and p = 0.04, respectively). Ore-R and Poxn-SuperA males also courted decapitated males intensely, yet with a cvi significantly reduced compared to that towards decapitated females (Figure 4C; p<0.001 for both cases).

pone-0004457-g004: Gustatory, but not olfactory, signals of the courted fly contribute to the heterosexual orientation of the courting male.(A) The fraction of males initiating courtship, (B) the average latency (in seconds) till courtship initiation, and (C) the courtship vigor index were measured in single-choice courtship assays, performed under dim red light with courting males of indicated genotypes and decapitated receptive Ore-R virgins (V, filled columns) or decapitated mature Ore-R males (♂, hatched columns).

Mentions:
To assess the importance of the different senses for the sexual orientation of males, we first observed males in single-choice courtship assays in the dark with object animals that had been decapitated to prevent their feedback behavior. All Ore-R and Poxn-SuperA control males initiated courtship towards decapitated females (Figure 4A) with a short latency (Figure 4B) and courted them vigorously until the end of observation (Figure 4C). Copulation with decapitated females was never observed even though males bent their abdomen and attempted to copulate, which suggests that positive feedback from the female is crucial for copulation (M13). When confronted with decapitated males, the fraction of Ore-R and Poxn-SuperA males initiating courtship was somewhat reduced (Figure 4A; p = 0.008 and p = 0.1, respectively, for comparison of courtship towards decapitated females and males), and the courtship latency significantly increased (Figure 4B; p = 0.006 and p = 0.04, respectively). Ore-R and Poxn-SuperA males also courted decapitated males intensely, yet with a cvi significantly reduced compared to that towards decapitated females (Figure 4C; p<0.001 for both cases).

Bottom Line:
To understand how the underlying neural network controls this behavior, it is not sufficient to unravel its architecture, but also crucial to decipher its logic.By systematic analysis of how variations in sensory inputs alter the courtship behavior of a naïve male in the single-choice courtship paradigm, we derive a model describing the logic of the network that integrates the various sensory stimuli and elicits this complex innate behavior.This approach and the model derived from it distinguish (i) between initiation and maintenance of courtship, (ii) between courtship in daylight and in the dark, where the male uses a scanning strategy to retrieve the decamping female, and (iii) between courtship towards receptive virgin females and mature males.

Affiliation:
Institute for Molecular Biology, University of Zürich, Zürich, Switzerland.

ABSTRACTThe courtship behavior of Drosophila melanogaster serves as an excellent model system to study how complex innate behaviors are controlled by the nervous system. To understand how the underlying neural network controls this behavior, it is not sufficient to unravel its architecture, but also crucial to decipher its logic. By systematic analysis of how variations in sensory inputs alter the courtship behavior of a naïve male in the single-choice courtship paradigm, we derive a model describing the logic of the network that integrates the various sensory stimuli and elicits this complex innate behavior. This approach and the model derived from it distinguish (i) between initiation and maintenance of courtship, (ii) between courtship in daylight and in the dark, where the male uses a scanning strategy to retrieve the decamping female, and (iii) between courtship towards receptive virgin females and mature males. The last distinction demonstrates that sexual orientation of the courting male, in the absence of discriminatory visual cues, depends on the integration of gustatory and behavioral feedback inputs, but not on olfactory signals from the courted animal. The model will complement studies on the connectivity and intrinsic properties of the neurons forming the circuitry that regulates male courtship behavior.